Data from: Species selection favors dispersive life histories in sea slugs, but higher per-offspring investment drives shifts to short-lived larvae

For 40 years, paleontological studies of marine gastropods have suggested that species selection favors lineages with short-lived (lecithotrophic) larvae, which are less dispersive than long-lived (planktotrophic) larvae. Although lecithotrophs appeared to speciate more often and accumulate over time in some groups, lecithotrophy also increased extinction rates, and tests for state-dependent diversification were never performed. Molecular phylogenies of diverse groups instead suggested lecithotrophs accumulate without diversifying due to frequent, unidirectional character change. Although lecithotrophy has repeatedly originated in most phyla, no adult trait has been correlated with shifts in larval type. Thus, both the evolutionary origins of lecithotrophy and its consequences for patterns of species richness remain poorly understood. Here, we test hypothesized links between development mode and evolutionary rates using likelihood-based methods and a phylogeny of 202 species of gastropod molluscs in Sacoglossa, a clade of herbivorous sea slugs. Evolutionary quantitative-genetics modeling and stochastic character mapping supported 27 origins of lecithotrophy. Tests for correlated evolution revealed lecithotrophy evolved more often in lineages investing in extra-embryonic yolk, the first adult trait associated with shifts in development mode across a group. However, contrary to predictions from paleontological studies, species selection actually favored planktotrophy; most extant lecithotrophs originated through recent character change, and did not subsequently diversify. Increased offspring provisioning in planktotrophs thus favored shifts to short-lived larvae, which led to short-lived lineages over macroevolutionary time scales. These findings challenge long-standing assumptions about the effects of alternative life histories in the sea. Species selection can explain the long-term persistence of planktotrophy, the ancestral state in most clades, despite frequent transitions to lecithotrophy.四十年来，海洋腹足类（marine gastropods）的古生物学研究一直认为，物种选择（species selection）更青睐具有短命卵黄营养型（lecithotrophic）幼虫的演化支——这类幼虫的扩散能力弱于长命浮游营养型（planktotrophic）幼虫。尽管在部分类群中，卵黄营养类群似乎有着更高的成种速率并随时间累积，但卵黄营养型发育同时也会提高灭绝速率，且此前从未有研究针对依赖状态的分化（state-dependent diversification）开展检验。相较之下，不同类群的分子系统发育（molecular phylogenies）研究表明，卵黄营养类群的累积并非源于分化，而是频繁的单向性状转变（character change）所致。尽管在绝大多数动物门（phylum）中，卵黄营养型发育已多次独立起源，但目前尚未发现任何成体性状与幼虫类型的转变存在关联。因此，卵黄营养型发育的演化起源及其对物种丰富度格局的影响，至今仍未得到清晰阐释。本研究基于似然法（likelihood-based methods），结合囊舌类（Sacoglossa，一类植食性海蛞蝓的演化支）202种腹足类软体动物的系统发育树，检验了发育模式与演化速率之间的假说关联。演化数量遗传学建模（evolutionary quantitative-genetics modeling）与随机性状映射（stochastic character mapping）结果支持，卵黄营养型发育曾独立起源27次。相关性演化检验显示，卵黄营养型发育更常在具有胚胎外卵黄（extra-embryonic yolk）投资的类群中演化——这是首个在类群水平上与发育模式转变相关的成体性状。然而，与古生物学研究的预测相悖，物种选择实际上更青睐浮游营养型发育：多数现存卵黄营养类群均通过近期的性状转变起源，且后续并未发生分化。因此，浮游营养类群中更高的后代抚育投入，反而推动了向短命幼虫的演化转变，进而在宏观演化时间尺度上形成了短命的演化支。本研究结果挑战了学界关于海洋中不同生活史模式影响的长期固有认知。尽管频繁发生向卵黄营养型发育的演化转变，但物种选择可以解释浮游营养型发育——多数类群的祖先性状状态（ancestral state）——的长期存续。